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Pollen morphology supports the reinstatement of Bergera (Rutaceae)

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Abstract

Pollen morphology of 11 species of Murraya and Micromelum (Clauseneae: Rutaceae) was investigated using scanning electron microscopy (SEM) and palynological characters including pollen size, aperture number and exine ornamentation were evaluated. The results indicate that species in M. sect. Bergera and sect. Murraya have very distinct pollen morphology. Species in section Bergera have rugulate to foveolate exine, whereas the tectum in section Murraya is cross-striate. This supports the redefinition of the genus Murraya, retaining only the species of section Murraya, while M. sect. Bergera is better treated as a separate genus. From the palynological point of view, it is suggested that Bergera and Murraya s.s. are not closely related, with the latter being more close to Micromelum and Merrillia, a result in accordance with phytochemical, chromosomal and molecular evidence, thus supporting the reinstatement of the generic name Bergera L.

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... According to Swingle and Reece (1967), , Samuel et al. 2001, palynology (Mou and Zhang 2009), chromosome (Guerra et al. 2000) and molecular phylogenety (Samuel et al. 2001, Pfeil and Crisp 2008, Bayer et al. 2009, Morton 2009). In the newest family treatment of Rutaceae, Kubitzki et al. (2011) defined the Bergera Alliance that includes Clausena, Bergera, Micromelum and Glycosmis. ...
... The current classifications of Clausena are mainly based on morphology (Swingle andReece 1967, Molino 1994). Pollen morphology has provided very useful taxonomic evidence in Rutaceae (Liu 1987, Grant et al. 2000, Mou and Zhang 2009). Liu (1987) reported that pollen grains of Rutaceae were colporate and four species of Clausena belonged to the 3-colporate with reticulate exine ornamentation type. ...
... Bergera and cross-striate in Murraya sect. Murraya being, Mou and Zhang (2009) treated sect. Bergera as a separate genus and suggested that Murraya s.s. was more close to Micromelum and Merrillia. ...
Article
Clausena is the most widely distributed genus in the subfamily Aurantioideae of the family Rutaceae. Morphological features of pollen grains from 10 species and two varieties of Clausena in China were examined using scanning electron microscopy (SEM). The pollen grains are small to medium in size and subprolate in shape, with a few being prolate. The apertures are usually 3-colporate, except one species (C. lansium) being 3- or 4-colporate. The morphology of the pollen grains shows significant variation in the exine ornamentation, viz. striato-reticulate, striate, rugulo-reticulate or striato-perforate. Five species and two varieties, viz. C. anisum-olens, C. dunniana var. dunniana, C. excavata var. excavata, C, inolida, C. lansium, C odorata and C. vestita commonly show the exine ornamentation of striato-reticulate type, but the width of murus and lumen vary between species. C. lenis and C. yunnanensis have the rugulo-reticulate exine ornamentation while C. excavata var. quadrangulata and C. dunniana var. robusta with C. emarginata are characterized with striate and striato-perforate exine ornamentation respectively. Clausena is eurypalynous and the pollen characteristics appear to be informative and useful for distinguishing species and for elucidating the relationships among some species.
... Murraya is the sister of Merrillia and has a more close relationship with the tribe Citreae. The same pattern may also be seen in morphological (Tanaka 1929, Swingle and Reece 1967), palynological (Grant et al. 2000, Mou andZhang 2009b) and phytochemical differences , Kong et al. 1988, Samuel et al. 2001, as well as cytology (Guerra et al. 2000) and DNA data (Samuel et al. 2001, Groppo et al. 2008, Bayer et al. 2009). Based on studies of heterochromatin banding patterns in the subfamily Aurantioideae, Guerra et al. (2000) proposed to divide Murraya s.l. ...
... Bergera with rugulate to foveolate exine ornamentation and sect. Murraya with cross-striate exine (Mou and Zhang 2009b). ...
... Based on all these studies, the genera Murraya and Bergera have previously been treated separately (Kubitzki et al. 2011). Therefore, it is proposed to restore the genus Bergera Koenig ex L. (Mou and Zhang 2009b) to accommodate members of Murraya sect. Bergera. ...
Article
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The data matrix in this study contained 91 accessions, 72 species or varieties from 31 genera and two outgroups, including new and extensive sampling of 43 accessions from 29 species or varieties representing four genera in the tribe Clauseneae. Using maximum likelihood (ML) and Bayesian inference (BI) methods, the phylogeny of Clauseneae was reconstructed based on trnL-F, atpB-rbcL and ITS. Six major clades were recognized with strong support in the subfamily Aurantioideae: (1) MICROMELUM Clade: Micromelum; (2) GLYCOSMIS Clade: Glycosmis; (3) BERGERA Clade: Murraya sect. Bergera; (4) CLAUSENA Clade: Clausena; (5) MURRAYA Clade: Murraya sect. Murraya, Merrillia; (6) CITREAE Clade: Citreae. Five genera of Clauseneae don't cluster together; four genera, namely Micromelum, Glycosmis, Clausena and Merrillia are monophyly respectively. However, the genus Murraya s.l. is recovered to be polyphyletic, in that Murraya sect. Bergera and Clausena form a separated branch while Murraya sect. Murraya and Merrillia are clustered into a group and is sister to the tribe Citreae. All members from Citreae are clustered into a natural group. The genus Micromelum is primitive group in this subfamily and more close to Glycosmis. Based on the phylogeny and other morphologic characters, the taxonomy of some major species from Clauseneae was also discussed here. The current tribal and generic classification need further revision, and additional studies are advisable before carrying out further taxonomic changes.
... Murraya consists of two groups of species that were assigned to the two sections Bergera J.Koenig and Murraya by Tanaka (1929). Phytochemical (Kong et al., 1988;But et al., 1986) and morphological (Mou and Zhang, 2009) studies confirmed the presence of two separate groups, which led Mou and Zhang (2009) to propose the reinstatement of the genus Bergera. The six genera contain a total of about 85 species (Kubitzki et al., 2011). ...
... Murraya consists of two groups of species that were assigned to the two sections Bergera J.Koenig and Murraya by Tanaka (1929). Phytochemical (Kong et al., 1988;But et al., 1986) and morphological (Mou and Zhang, 2009) studies confirmed the presence of two separate groups, which led Mou and Zhang (2009) to propose the reinstatement of the genus Bergera. The six genera contain a total of about 85 species (Kubitzki et al., 2011). ...
Article
The Clauseneae (Aurantioideae, Rutaceae) is a tribe in the Citrus family that, although economically important as it contains the culinary and medicinally-useful curry tree (Bergera koenigii), has been relatively understudied. Due to the recent significant taxonomic changes made to this tribe, a closer inspection of the genetic relationships among its genera has been warranted. Whole genome skimming was used to generate chloroplast genomes from six species, representing each of the four genera (Bergera, Clausena, Glycosmis, Micromelum) in the Clauseneae tribe plus one closely related outgroup (Merrillia), using the published plastome sequence of Citrus sinensis as a reference. Phylogenetically informative character (PIC) data was analyzed using a genome alignment of the seven species, and variability frequency among the species was recorded for each coding and non-coding region, with the regions of highest variability identified for future phylogenetic studies. Non-coding regions exhibited a higher percentage of variable characters as expected, and the phylogenetic markers ycf1, matK, rpoC2, ndhF, trnS-trnG spacer, and trnH-psbA spacer proved to be among the most variable regions. Other markers that are frequently used in phylogenetic studies, e.g. rps16, atpB-rbcL, rps4-trnT,and trnL-trnF, proved to be far less variable. Phylogenetic analyses of the aligned sequences were conducted using Bayesian inference (MrBayes) and Maximum Likelihood (RAxML), yielding highly supported divisions among the four genera.
... Therefore, knowledge about pollen traits of species and cultivars is one of the main issues for growers and also for breeding programs, especially in grapevines (Lombardo et al., 1976;Carmona et al., 2008;Bautista et al., 2008). The palynology has presented considerable opportunities for cultivar identification in grapevines and not only, besides its importance in plant taxonomy (Cabello-Saenz-Santa-Maria et al., 1994;Inceoğlu et al., 2000;Marasali et al., 2005;Mou and Zhang, 2009). Genotypes of grapevine with poor quality pollens, such as sterile pollens, pollen with low germination percentage or low tube growth rate versus cultivars with high pollen germination and tube growth have been reported (Kevan et al., 2011). ...
Article
Full-text available
Noah and Othello cultivars are American direct producer hybrids with different genetic origins. Noah is native of Vitis labrusca × Vitis riparia and Othello of (Vitis labrusca × Vitis riparia) × Black Hamburg (Vitis vinifera). Their grape productions are different. Pollen quality is important for grape production. Present research studied the two direct producer hybrids in order to highlight the pollen qualities correlated to genetic substrate of genitors. It presents a holistic approach of the two direct producer hybrids’ pollen, including a brief palynological characterization, germination potential analysis, dynamics of pollen tube growth, stages of pollen tube edification, morphological abnormalities of pollen tubes and main floral elements. The correlations between these characteristics can be used at the grape production appreciation based on pollen quality. Palynological characteristics of the two direct producer hybrids are very similar, as they belong to Vitis genus, even if the genitors are different. Germination potential is higher for Othello cultivar. In vitro, the pollen tube growth is fast and increases significantly within the first 24 h on mediums with 15% and 25% sucrose. It is proved that the longest pollen tubes are correlated with style's length of the flower of the two genotypes. Pollen tube abnormalities are more frequent in Noah than in Othello.
... According to phylogenetic analyses of the subfamily Aurantioideae based on non-coding plastide DNA sequences the classical subdivision into tribes Clauseneae and Citreae is only justified if the genus Murraya (exclusive the species segregated as Bergera) is transferred to the tribe Citreae (Samuel et al. 2001;But et al. 2009). The reinstatement of Bergera as a separate genus is also supported by pollen morphology (Mou and Zhang 2009) and analysis of chloroplast genomes (Shivakumar et al. 2016). In view of the chemical characters the genus Micromelum takes a somewhat intermediate position containing carbazoles as well as 8-prenylated coumarins and polyoxygenated flavonoids (Bowen and Perera 1982;Kong et al. 1988b;Grassi 1998). ...
Article
Full-text available
Carbazole alkaloids characterized by a heterocyclic aromatic basic skeleton are known from different organisms but do not represent a biogenetically homogenous group. The majority, comprising more than 330 derivatives, is derived from 3-methylcarbazole as common precursor and is designated as phytocarbazoles. They are nearly exclusively known from the four closely related plant genera Bergera (part of Murraya s. l.), Clausena, Glycosmis, and Micromelum of the family Rutaceae. Derived from anthranilic acid and malonyl-CoA the tricyclic basic skeleton is formed via a prenylated 2-quinolone intermediate. The following steps are speculated to involve the formation of 2-prenylindole and cyclization of the prenyl side chain to generate 3-methylcarbazole. Apart from different oxygenations and oxidations of the basic skeleton additional prenylations and geranylations contribute to the great structural diversity of phytocarbazoles which are grouped together according to their C13-, C18-, and C23-basic structures. Of taxonomic significance are the different oxidations of the characteristic C-3 methyl group leading to 3-formyl- and 3-carboxyl derivatives particularly accumulated in Clausena and Micromelum species. Predominant prenylation at C-5 is typical for Glycosmis and Micromelum, whereas in Clausena prenylation at different positions can contribute to an infrageneric grouping. Geranylation represents a characteristic biogenetic trend of Bergera. A wide variety of biological activities ranges from significant antimicrobial, antiprotozoal, and insecticidal properties to anti-inflammatory, antioxidative, antiplatelet aggregative, and anti-HIV activities. Of particular interest is the cytotoxicity of phytocarbazoles against various cancer cell lines, where some derivatives turned out to act as cell cycle inhibitors and apoptosis inducers. Especially the C23 derivative mahanine induced different cell-signaling pathways suggesting that it represents a multi-targeted and multi-functional compound that works on an array of different cancer types and has the potential to inhibit tumor growth in vivo.
... The pollen morphology of different species of Rutaceae has been described by Erdtman (1952), Sato (1971), Barth (1980Barth ( , 1982Barth ( , 1983Barth ( , 1985, Arreguin-Sanchez et al. (1986), Roubick & Moreno (1991), Corrêa et al. (1992), Mziray (1992), Breis et al. (1993), Morton & Kallunki (1993), Victor & Van Wyk (1998, 1999a, 1999b, 2001, Grant et al. (2000), Carreira & Barth (2003), Qaiser & Perveen (2005), Magalhães-e-Silva (2007), Fukuda et al. (2008), Mou & Zhang (2009), Groppo et al. (2010, Cao et al. (2014), Radaeski et al. (2014), Silva et al. (2014) and Al-Anbari et al. (2015). These authors observed the differences in the morphology of the pollen grains of the species studied, especially regarding the aperture, shape and ornamentation of the exine, concluding that the family is eurypalynous. ...
Article
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This paper presents pollen morphology of 12 native Brazilian species of Rutaceae from forest fragments of São Paulo, Brazil. The aim of this research is to expand the morphological knowledge of the species, thus contributing to taxonomic knowledge and, subsequently, conservation of species and the forest area. The pollen grains were acetolyzed, measured, described qualitatively, and illustrated using light microscopy (LM) and scanning electron microscopy (SEM). The studied species have differences in polarity, size, shape, aperture and exine ornamentation of the pollen grains, confirming the eurypalynous character of Rutaceae pollen. In particular, species of Zanthoxylum L. also presented significant differences in the pollen grains, confirming the morphological variation within the genus. The quantitative data and multivariate analysis confirm the morphological description; thus, the results reinforce the importance of pollen morphology in the identification and characterization of species of Rutaceae.
... The differences and similarities in pollen morphology of some investigated species showed significant evidences and could be exploited for biosystematic purposes. Mou and Zhang [2] investigated pollen morphology of eleven species of Murraya and Micromelum in the family Rutaceae. They indicated that species of M. sect. ...
Article
Palynological features of C. sinensis, C. limon, C. aurantifolia, C. paradisi, C. reticulata and C. maxima collected from various parts of Owerri were examined and evaluated in order to determine the taxonomic value of the observed internal peculiarities. Features related to pollen shape showed circular to elliptic shapes in all the taxa while rectangular shape distinguished C. limon, C. paradise and C. maxima. Polar view showed that C. paradisi and C. maxima have closer affinity than the other taxa studied. Palynological characters as observed in this study were found useful especially in delimiting the investigated taxa and thus could be exploited in conjunction with other evidences in specie identification and characterization.
... The pollen morphology of Rutaceae has similarly received considerable attention as an important character in interpreting systematic relationships (Morton & Kallunki, 1993;Victor & Van Wyk, 1998, 1999, 2001Grant et al., 2000;Mou & Zhang, 2009). Barth (1980) examined 17 species of Zanthoxylum in Brazil, and concluded that the pollen type is homogeneous in this genus. ...
Article
Pollen grains of 32 species of Zanthoxylum were studied under light microscopy and scanning electron microscopy. The macro-and micro-morphological pollen characters, including shape, pollen size, aperture and exine ornamentation type were examined. The pollen grains are small to medium in size, mostly from subspheroidal to prolate shape in equatorial view and 3–lobed circular in polar view. Three types are recognized based on exine ornamentation, includes macroreticulate, parallel striation, and striate-rugulate. Pollen shape and size are found to have only minor value, but pollen exine ornamentation contains useful information on modify the Englerian classification of Zanthoxylum and can be used for identifying different species of Zanthoxylum s.l.. Based on the pollen morphological data, the two subgenus, Fagara and Zanthoxylum, should be combined.
... Recent palynological studies suggested that the genus Murraya s.l. should be divided into two genera, Murraya and Bergera (Mou & Zhang, 2009b), in accordance with earlier phytotaxonomical and phylogenetic studies on the group (Guerra et al., 2000; Samuel et al., 2001; Bayer et al., 2009). ...
Article
Chromosome numbers for 21 Rutaceous species, representing five genera (Bergera, Clausena, Glycosmis, Micromelum, and Murraya) in the tribe Clauseneae (Aurantioideae, Rutaceae) were investigated to shed light on the relationships between these genera in the tribe in particular, and with other groups in the orange subfamily in general. Most species have the chromosome number 2n = 2x = 18, but Glycosmis shows variable chromosome numbers with ploidy levels ranging from 2x to 8x. Glycosmis parviflora is hexaploid with a chromosome number of 2n = 6x = 54 and G. longipetala octoploid with 2n = 8x = 72, and diploid with 2n = 2x = 18 was observed in other species. One species (Clausena excavata) shows intraspecies ploidy variation. The chromosome numbers of 11 species, Bergera kwangsiensis, B. microphylla, Clausena dunniana, C. emarginata, C. lenis, C. yunnanensis, Glycosmis esquirolii, G. lucida, G. oligantha, Micromelum falctum, and Murraya alata, are reported for the first time. The basic chromosome number x = 9 was inferred for all species studied. These results, together with previous chromosome counts in the tribe Citreae, reveal a cytological homogeneity, and strongly support the monophyly of the orange subfamily.
Article
A new species, Bergera unifolia C.L. Deng & F.J. Mou (Rutaceae, Aurantioideae, Clauseneae) is described and illustrated from Dahua County, Guangxi Province, China, based on morphological characters as well as on nrDNA (ITS) and cpDNA (trnL-F, atpB-rbcL, rbcL, matK, psbH-petB and psbA-trnH) sequences. It is characterised by unifoliate leaves similar to those of Murraya stenocarpa (Murraya sect. Bergera, or Chalcas sect. Bergera) but differs from it by having smaller and thinner subcoriaceous leaflets with irregularly toothed margins. The leaflets resemble those of M. kwangsiensis (Murraya sect. Bergera) in having hairs under the leaflets, oil glands and similar odour. Based on molecular data, B. unifolia is closely related to M. stenocarpa and M. kwangsiensis and thus it is important for resolving the classification of those species within Murraya sect. Bergera that should be formally transferred to Bergera.
Chapter
Trees or shrubs, sometimes scandent, rarely herbs, sometimes spiny or aculeate, usually (but not in all Cneoroideae) with schizogenous (mostly pellucid) glands containing volatile oils on leaves, young branchlets, inflorescences, flower parts, pericarp and cotyledons, and with oil cells in parenchymatous tissue; cork subepidermal. Leaves alternate, opposite, or whorled, entire or toothed, variously compound, unifoliolate, or simple, the rhachis sometimes winged; stipules 0. Inflorescences panicles, thyrses, racemes, spikes, botryoids, sciadioids, heads, umbels, or cincinni. Flowers bisexual or unisexual, usually 3–5-merous, actinomorphic or rarely somewhat zygomorphic, hypogynous or sometimes perigynous; sepals distinct to completely connate; petals distinct or sometimes coherent or connate for part of their length; stamens twice the number of petals or equal to it or sometimes more numerous (50–100 in Clymenia), obdiplostemonous, the antepetalous stamens often transformed into staminodia or 0; filaments distinct or sometimes coherent or connate for part of their length; anthers 4-sporangiate, longitudinally dehiscent, introrse or sometimes latrorse; disk (sometimes 0) intrastaminal, nectariferous; gynoecium often inserted on gynophore, of 1–5(–many) carpels, ranging from more or less apocarpous with distinct or only proximally connate ovarioles and stylodia usually joined in a common style or at least with joined stigmas to completely syncarpous; each carpel with 1 locule and 1–several (rarely many) ovules; ovules bitegmic or very rarely (Glycosmis) unitegmic, crassinucellar, anatropous or hemitropous, more or less epitropous; placentation axile, very rarely parietal.
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The Aurantioideae is one of seven subfamilies of the Rutaceae consisting of two tribes, the Clauseneae, containing five genera, and the Citreae, with 28 genera. Each tribe contains three subtribes. The pollen morphology of the subfamily Aurantioideae is described and illustrated for the first time based on light and scanning electron microscopy. Five pollen types have been recognised in the subfamily, based mainly on aperture number and exine ornamentation. The pollen grains show a high degree of intergeneric variation. Pollen grains of Clauseneae are 3-colporate, microstriate or microstriato-reticulate, whereas pollen grains of Citreae are almost always 4/5 colporate with exines varying from microperforate to coarsely reticulate. Congruence between pollen types and the currently accepted classification is discussed, as well as the systematic implications of pollen morphology for the subfamily.
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Primarily known only by the edible fruits of Citrus, Rutaceae comprise a large (c. 160 genera and 1900 species), morphologically diverse, cosmopolitan family. Of its extraordinary array of secondary chemical compounds, many have medicinal, antimicrobial, insecticidal, or herbicidal properties. To assist with the much-needed suprageneric reclassification and with studies of evolution of chemical compounds and biogeographic history of the family, here we included sequence data (from two noncoding regions of the chloroplast genome-rps16 intron and trnL-trnF region) from 65 species in 59 genera (more than one third of those in the family) that represented all subfamilies and tribes and more genera of Toddalioideae and of neotropical groups than previous studies. Results confirmed that Cneorum, Ptaeroxylon, Spathelia, and Dictyoloma form a clade sister to the remaining Rutaceae, none of the subfamilies with more than one genus (except Aurantioideae) is monophyletic, and characters of the ovary and fruit are not reliable for circumscription of subfamilies. Furthermore, clades are better correlated with geographic distributions of the genera than with ovary and fruit characters. Circumscriptions of subfamilies and tribes (and some subtribes of Rutoideae) must be reevaluated. Results are discussed in light of geographic distributions, caryology, chemotaxonomy, and other molecular studies.
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From the stem and root barks of Merrillia caloxylon (Rutaceae) the dimeric indole alkaloid yuehchukene has been isolated together with a simple prenylated indole, the 8-prenylated coumarins sibiricin and phebalosin, and the polyoxygenated flavonoid, eupatorin. The finding of these three classes of metabolites in Merrillia strongly supports Swingle in his proposal that this taxon is closely allied to Murraya paniculata, a member of Murraya section Murraya. The possible significance of these findings for the phylogeny of the tribe Clauseneae is explored and their implications for predicting the potential distribution of yuehchukene in the Aurantioideae is discussed.
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An examination of the roots of eight species and one variety of Murraya for the presence of the dimeric indole yuehchukene has revealed a dichotomy in the genus between species producing this alkaloid and those producing the carbazole alkaloid girinimbine, with no apparent overlap between the two groups of species.
Pollen morphology of the family Rutaceae in China
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Erdtman, G. 1969. Handbook of palynology (morphologyÁ taxonomyÁecology) an introduction to the study of pollen grains and spores. Á Munksgaard.
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Linnaeus, C. A. 1771. Mantissa plantarum. Altera generum editionis VI et specierum editionis II. Á Impensis Direct. Laurentii Salvii.
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Flora Reipublicae Populais Sinicae. Tomus 43. Angiospermae Dicotyledoneae Rutaceae
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Á(33) Micromelum falcatum, (34)Á(36) M. integerrimum. Scale bars: (25)Á(26), (31)Á (32), (34), (35) 010 mm, (28)Á(29), (33) 05 mm
  • M Omphalocarpa
Á(30) M. paniculata var. omphalocarpa, (31)Á(33) Micromelum falcatum, (34)Á(36) M. integerrimum. Scale bars: (25)Á(26), (31)Á (32), (34), (35) 010 mm, (28)Á(29), (33) 05 mm, (27), (36) 02 mm, (30) 01 mm.
Preliminary study on Chinese Rutaceae (3)
  • Huang